This discussion topic submitted by Malcolm Schongalla (
c01malcolm.schongall@usafa.af.mil) at 11:38 pm on 5/8/01. Additions were last made on Saturday, May 4, 2002.
INTRODUCTIONThe red mangrove (Rhizophora mangle) and the black mangrove (Avicennia germinans) are two common new-world mangroves which employ different strategies for coping with salt. This paper will examine the current understanding of these strategies and how the strategies affect the plant. It is important to study these plants because mangroves are an economic and environmental resource in many tropical countries (Macintosh and Zisman, 1999). They provide, among other resources, food and habitat for animals above and below water level, soil stabilization, timber and firewood, charcoal, and tannin (Law and Arny, 2001; Macintosh and Zisman, 1999). Knowledge of these plants can assist wildlife managers in many parts of the world to properly manage and preserve the unique ecosystems which mangroves characterize.Mangroves face certain specific challenges to growth associated with tropical intertidal zones. Besides high salinity levels, mangroves must withstand fluctuating water levels, soft, anaerobic soil, the shade of other mangroves, and tropical storms (Tomlinson, 1986). Soft soil affects the ability of plants to prop them selves upright against forces such as gravity and wind. Groundwater salinity levels may also vary, and in some cases are significantly higher than seawater salinity levels (Morrow and Nickerson, 1973). Salt management is especially important because sodium can be toxic to plants. Also, ion concentrations affect osmotic potentials, making it difficult to draw water up to the leaves.RED MANGROVEThe red mangrove is one of the most prolific new-world mangroves, inhabiting coasts on both sides of the Atlantic ocean, as well as the eastern Pacific ocean and areas of Melanesia and Polynesia (SMSFP 2001b; Tomlinson, 1986). Rhizophora mangle is often the most seaward-growing species of mangrove in Caribbean and Atlantic mangrove forests (SMSFP 2001b). It is also one of the tallest, growing more than 22 m. It is easily identified by its "walking" stilt roots that can grow as high as 4.5 m above ground (PUCNCPP, 1983b). Like the black mangrove, the edge of the red mangrove habitat matches the 20¡C isotherm, at approximately 28¡ north and south. It can tolerate a range of salinity from freshwater to sea water, and as such is considered a facultative halophyte (SMSFP, 2001b; PUCNCPP, 1983b).Rhizophora mangle is considered a non-secreting salt excluder because it excludes salt from entering the roots and lacks glandular secretory structures. The salt in xylem sap of R. mangle is 100 times less concentrated than in seawater (Tomlinson, 1968; Scholander, 1968; Scholander et. al., 1962). It is generally agreed that this is accomplished by a process of ultrafiltration in the cell membranes of roots (Werner and Stelzer, 1989; Tomlinson, 1986; Field, 1984; Scholander, 1968). Evidence from Scholander (1968) suggests that the filtration process is physical in nature (as opposed to metabolic) because it is unaffected by factors that would commonly inhibit metabolic processes, such as toxins or extreme temperatures. Speculation in the literature seems to favor radial filtration across the cells of the root endodermis, cortex, and epidermis (Werner and Stelzer, 1989; Tomlinson, 1986).One osmotic regulation model proposed by Werner and Stelzer (1989) involves three primary points of regulation. The first is a radial filtration process in the cells of the root cortex. This prevents the majority of salts from entering the plant. Second is an Na+/K+ ion exchange system in xylem or hypocotyl cells. Third is an Na+/K+ ion

exchange system in leaves. Any Na+ ions that evade the filtration system are thus gradually pushed back downwards to the roots. Figure 1 (from Werner and Stelzer, 1989) depicts Na+ and K+ concentrations measured at various layers of root tissue, starting at the growth medium and going inwards to the xylem vessels. The general trend seems that most Na+ and Cl- ions are filtered at the epidermis, and generally exhibit decreasing concentrations further inward. Werner and Stelzers' model includes the trapping of ions in the vacuoles of cortex cells. Each successive layer of the cortex is exposed to a lower concentration of ions. As the root elongates, ion-saturated filter cells are sealed by suberinization. Sodium ions that penetrate the ultrafilter must next pass through the xylem and the hypocotyl. Here Werner and Stelzer hypothesize ion pumps that act as a second Na+ barrier by transporting Na+ back down in exchange for K+ ions transported upwards. The third barrier is a similar ion exchange process inside the leaves.This model suggests that metabolic processes play some role in overall salt regulation, in contradict Scholander's findings. Although Werner and Stelzer do not offer a complete explanation of the ultrafiltration mechanism, they offer a plausible model that can be tested experimentally.BLACK MANGROVE Unlike the red mangrove, the black mangrove secretes excess salt through specialized glands on the surface of leaves in addition to carrying out root ultrafiltration. In the western Atlantic and Caribbean A. germinans typically grows further inland than R. mangle, often between zones of red and white mangroves (Laguncularia racemosa) (FMRI, 2001; SMSFP, 2001). The black mangrove is nearly as tall as the red mangrove, reaching heights of 15-20 m (Law and Arny, 2001; NHMI, 2001). Its root system employs pneumatophores rather than stilt roots (Figure 2). The black mangrove is found in the western Atlantic, Bahamas, Gulf of Mexico, and on the eastern Pacific coast including Ecuador, Peru, and Galapagos Islands (SMSFP, 2001; Dodd et. al., 2000; PUCNCPP, 1983a). The black mangrove is often found in more saline environments than the red mangrove, although their distributions may overlap across salinity gradients (Morrow and Nickerson, 1973).

Black mangrove roots can filter 90% of the salt from sea water (Tomlinson, 1986; Scholander, 1968), although some investigators report considerably smaller percentages, some as low a 30% (Field, 1984). To cope with the additional salt, the salt glands secrete solutions that evaporate, leaving behind salt crystals on the leaf surface (Tomlinson, 1986; Scholander et. al., 1962). Salt glands are microscopic and occur in epidermal depressions on the upper leaf surface. Each gland has 8-12 outer secretory cells, a lower stalk cell, and two to four other subtending, or basal cells, enclosed in a cuticle (Figure 3) (Dschida et. al., 1992). Evidence suggests that these salt glands, unlike the ultrafilter of R. mangle, rely on metabolic processes to function. The gland cells have elevated numbers of mitochondria, ribosomes, and other organelles (Tomlinson, 1986). They are impeded by metabolic inhibitors, implying a dependence on an energy source such as ATP (Dschida et. al., 1992).

Based on analysis of the application of specific metabolic inhibitors, Dschida et. al. (1992) suggest ions are actively transported from mesophyll cells into the gland across the basal cell membrane. Their analysis also suggests that mitochondria provide the energy source for sustaining secretion. Furthermore, it is highly possible that "an electrochemical potential established by H+ ATPase underlies the secretory process" (Dschida et. al., 1992).Dschida et. al. also investigated the relationship of glandular secretion to changes in physiological inputs. Peels of adaxial leaf surfaces were floated on treatment solutions containing various concentrations of NaCl, and exposed to different temperatures. Volume of secretion varied directly with temperature, and varied indirectly with NaCl concentration. The rate of Cl- secretion peaked at a NaCl concentration of approximately 100 mol m-3 (Figure 4). These findings suggest the salt glands respond to the need to conserve water under saline conditions by secreting Cl- more efficiently. It would be interesting to compare the NaCl concentration of xylem sap reaching the leaves to the NaCl concentration of peak Cl- secretion reported by these investigators.COMPARISON OF STRATEGIESSome of the main differences between the mangroves include the types of mechanisms employed, the effectiveness of mechanisms, metabolic requirements, and osmotic potential of xylem sap. Based on the literature reviewed, the salt glands of A. germinans probably have a higher metabolic cost than the ultrafilter of R. mangle. This may be a factor in the zonation of these two species. For instance, R. mangle is often found closest to the coastline or in brackish water upstream from river mouths. Here one might expect the roots to encounter water that circulates more freely, preventing ion buildup around the roots. Further inland, where A. germinans is usually found, repeated inundations and draining can cause groundwater to become hypersaline (Morrow and Nickerson, 1973). The more saline the groundwater, the more negative the osmotic potential needed in the xylem sap of the tree to maintain water flow. Since R. mangle has a more effective ultrafilter, the water potential of its sap would be expected to be less negative. Indeed, xylem sap of A. germinans has an osmotic potential of ﷓300 to ﷓600 kPa, much lower than that of R. mangle, ﷓50 to ﷓150 kPa (Field, 1984). This could be a competitive disadvantage for the red mangrove in areas of especially high salinity. However, in seawater or brackish water, A. germinans has the competitive disadvantage of metabolically maintaining its salt glands. One should note that in some locations, such as the coast of Australia, species of the Rhizophora genus are typically found further inland than species of Avicennia, which is found at the water's edge. However R. mangle and A. germinans are not found in these locations (Tomlinson, 1986).CONCLUSIONDespite studies of both salt balance strategies, many fundamental questions remain. One area of uncertainty is the cellular process by which the roots of all mangroves, particularly of R. mangle, block salt. Salt glands of A. germinans are becoming better understood in many ways. The gland ultrastructure has been described but questions remain regarding processes inside the cells as well as ion transport from the secretory cells to the cuticle. Furthermore, models explaining water relations in mangroves in general are under debate (Field, 1984). While there is no doubt that salt balance plays an important part in the ecophysiology of these trees, numerous other factors are also important. Since many features of mangrove roots are adaptions to unique soil characteristics, such as stability, oxygen content, and flood-toleration (Tomlinson, 1986), variations in soil characteristics also play a part in mangrove distribution. True plant vivipary, unique to mangroves, would also have an impact on plant site selection. Any of these topics alone would provide an opportunity for in-depth research. Knowledge of all these factors contributes to a better overall understanding of mangrove ecology. These factors, in addition to salt regulation, undoubtedly play an important role in zonation of these mangroves.

ACKNOWLEDGEMENTS Dr. Hays Cummins provided the Macintosh and Zisman article as well as feedback on the original outline and sources.